Calcium-sensing receptor and CPAP-induced neonatal airway hyperreactivity in mice.


Journal

Pediatric research
ISSN: 1530-0447
Titre abrégé: Pediatr Res
Pays: United States
ID NLM: 0100714

Informations de publication

Date de publication:
05 2022
Historique:
received: 18 11 2020
accepted: 05 04 2021
revised: 15 03 2021
pubmed: 8 5 2021
medline: 18 6 2022
entrez: 7 5 2021
Statut: ppublish

Résumé

Continuous positive airway pressure (CPAP) in preterm infants is initially beneficial, but animal models suggest longer term detrimental airway effects towards asthma. We used a neonatal CPAP mouse model and human fetal airway smooth muscle (ASM) to investigate the role of extracellular calcium-sensing receptor (CaSR) in these effects. Newborn wild type and smooth muscle-specific CaSR CPAP increased airway reactivity in WT but not CaSR These data implicate CaSR in CPAP effects on airway function with implications for wheezing in former preterm infants. Neonatal CPAP increases airway reactivity to bronchoconstrictor agonist. CPAP increases smooth muscle expression of the extracellular calcium-sensing receptor (CaSR). Inhibition or absence of CaSR blunts CPAP effects on contractility. These data suggest a causal/contributory role for CaSR in stretch effects on the developing airway. These data may impact clinical recognition of the ways that CPAP may contribute to wheezing disorders of former preterm infants.

Sections du résumé

BACKGROUND
Continuous positive airway pressure (CPAP) in preterm infants is initially beneficial, but animal models suggest longer term detrimental airway effects towards asthma. We used a neonatal CPAP mouse model and human fetal airway smooth muscle (ASM) to investigate the role of extracellular calcium-sensing receptor (CaSR) in these effects.
METHODS
Newborn wild type and smooth muscle-specific CaSR
RESULTS
CPAP increased airway reactivity in WT but not CaSR
CONCLUSIONS
These data implicate CaSR in CPAP effects on airway function with implications for wheezing in former preterm infants.
IMPACT
Neonatal CPAP increases airway reactivity to bronchoconstrictor agonist. CPAP increases smooth muscle expression of the extracellular calcium-sensing receptor (CaSR). Inhibition or absence of CaSR blunts CPAP effects on contractility. These data suggest a causal/contributory role for CaSR in stretch effects on the developing airway. These data may impact clinical recognition of the ways that CPAP may contribute to wheezing disorders of former preterm infants.

Identifiants

pubmed: 33958714
doi: 10.1038/s41390-021-01540-4
pii: 10.1038/s41390-021-01540-4
pmc: PMC8571113
mid: NIHMS1692836
doi:

Substances chimiques

CASR protein, mouse 0
RNA, Small Interfering 0
Receptors, Calcium-Sensing 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1391-1398

Subventions

Organisme : NHLBI NIH HHS
ID : P01 HL107147
Pays : United States
Organisme : NIH HHS
ID : S10 OD024996
Pays : United States
Organisme : NIA NIH HHS
ID : R21 AG070721
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL056470
Pays : United States
Organisme : BLRD VA
ID : IK6 BX004835
Pays : United States
Organisme : BLRD VA
ID : I01 BX005851
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL138402
Pays : United States

Informations de copyright

© 2021. The Author(s), under exclusive licence to the International Pediatric Research Foundation, Inc.

Références

Baraldi, E., Carraro, S. & Filippone, M. Bronchopulmonary dysplasia: definitions and long-term respiratory outcome. Early Hum. Dev. 85, S1–S3 (2009).
pubmed: 19793629 doi: 10.1016/j.earlhumdev.2009.08.002
Jaakkola, J. J. et al. Preterm delivery and asthma: a systematic review and meta-analysis. J. Allergy Clin. Immunol. 118, 823–830 (2006).
pubmed: 17030233 doi: 10.1016/j.jaci.2006.06.043
Joshi, S. et al. Exercise-induced bronchoconstriction in school-aged children who had chronic lung disease in infancy. J. Pediatr. 162, 813–818 e811 (2013).
pubmed: 23110946 doi: 10.1016/j.jpeds.2012.09.040
Laughon, M. M. et al. Prediction of bronchopulmonary dysplasia by postnatal age in extremely premature infants. Am. J. Respir. Crit. Care Med. 183, 1715–1722 (2011).
pubmed: 21471086 pmcid: 3136997 doi: 10.1164/rccm.201101-0055OC
Mayer, C. A., Martin, R. J. & MacFarlane, P. M. Increased airway reactivity in a neonatal mouse model of continuous positive airway pressure. Pediatr. Res. 78, 145–151 (2015).
pubmed: 25950451 pmcid: 4506702 doi: 10.1038/pr.2015.90
McFawn, P. K. & Mitchell, H. W. Bronchial compliance and wall structure during development of the immature human and pig lung. Eur. Respir. J. 10, 27–34 (1997).
pubmed: 9032487 doi: 10.1183/09031936.97.10010027
Tepper, R. S., Wiggs, B., Gunst, S. J. & Pare, P. D. Comparison of the shear modulus of mature and immature rabbit lungs. J. Appl. Physiol. 87, 711–714 (1999).
pubmed: 10444631 doi: 10.1152/jappl.1999.87.2.711
Yang, Y. et al. Stretch-induced alternative splicing of serum response factor promotes bronchial myogenesis and is defective in lung hypoplasia. J. Clin. Invest. 106, 1321–1330 (2000).
pubmed: 11104785 pmcid: 387248 doi: 10.1172/JCI8893
Kitterman, J. A. The effects of mechanical forces on fetal lung growth. Clin. Perinatol. 23, 727–740 (1996).
pubmed: 8982567 doi: 10.1016/S0095-5108(18)30205-7
MacFarlane, P. M. et al. CPAP protects against hyperoxia-induced increase in airway reactivity in neonatal mice. Pediatr Res. https://doi.org/10.1038/s41390-020-01212-9 (2020).
Ramchandani, R. et al. Differences in airway structure in immature and mature rabbits. J. Appl. Physiol. 89, 1310–1316 (2000).
pubmed: 11007563 doi: 10.1152/jappl.2000.89.4.1310
Ramchandani, R., Shen, X., Gunst, S. J. & Tepper, R. S. Comparison of elastic properties and contractile responses of isolated airway segments from mature and immature rabbits. J. Appl. Physiol. 95, 265–271 (2003).
pubmed: 12794098 doi: 10.1152/japplphysiol.00362.2002
Prakash, Y. S. Airway smooth muscle in airway reactivity and remodeling: what have we learned? Am. J. Physiol. Lung Cell Mol. Physiol. 305, L912–L933 (2013).
pubmed: 24142517 pmcid: 3882535 doi: 10.1152/ajplung.00259.2013
Prakash, Y. S. Emerging concepts in smooth muscle contributions to airway structure and function: implications for health and disease. Am. J. Physiol. Lung Cell Mol. Physiol. 311, L1113–L1140 (2016).
pubmed: 27742732 pmcid: 5206394 doi: 10.1152/ajplung.00370.2016
Thompson, M. A. et al. cAMP-mediated secretion of brain-derived neurotrophic factor in developing airway smooth muscle. Biochim. Biophys. Acta 1853, 2506–2514 (2015).
pubmed: 26112987 pmcid: 4558218 doi: 10.1016/j.bbamcr.2015.06.008
Vogel, E. R. et al. Moderate hyperoxia induces extracellular matrix remodeling by human fetal airway smooth muscle cells. Pediatr. Res. 81, 376–383 (2017).
pubmed: 27925619 doi: 10.1038/pr.2016.218
Faksh, A. et al. Effects of antenatal lipopolysaccharide and postnatal hyperoxia on airway reactivity and remodeling in a neonatal mouse model. Pediatr. Res. 79, 391–400 (2016).
pubmed: 26539665 doi: 10.1038/pr.2015.232
Riccardi, D., Brennan, S. C. & Chang, W. The extracellular calcium-sensing receptor, CaSR, in fetal development. Best. Pract. Res. Clin. Endocrinol. Metab. 27, 443–453 (2013).
pubmed: 23856271 pmcid: 4462341 doi: 10.1016/j.beem.2013.02.010
Kovacs, C. S. & Kronenberg, H. M. Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr. Rev. 18, 832–872 (1997).
pubmed: 9408745
Brennan, S. C. et al. Calcium sensing receptor signalling in physiology and cancer. Biochim. Biophys. Acta 1833, 1732–1744 (2013).
pubmed: 23267858 doi: 10.1016/j.bbamcr.2012.12.011
Riccardi, D. & Kemp, P. J. The calcium-sensing receptor beyond extracellular calcium homeostasis: conception, development, adult physiology, and disease. Annu Rev. Physiol. 74, 271–297 (2012).
pubmed: 22017175 doi: 10.1146/annurev-physiol-020911-153318
Goltzman, D. & Hendy, G. N. The calcium-sensing receptor in bone–mechanistic and therapeutic insights. Nat. Rev. Endocrinol. 11, 298–307 (2015).
pubmed: 25752283 doi: 10.1038/nrendo.2015.30
Patel, B. S., Ravix, J., Pabelick, C. & Prakash, Y. S. Class C GPCRs in the airway. Curr. Opin. Pharm. 51, 19–28 (2020).
doi: 10.1016/j.coph.2020.04.002
Brauner-Osborne, H., Wellendorph, P. & Jensen, A. A. Structure, pharmacology and therapeutic prospects of family C G-protein coupled receptors. Curr. Drug Targets 8, 169–184 (2007).
pubmed: 17266540 doi: 10.2174/138945007779315614
Hannan. F. M., Olesen, M. K. & Thakker R. V. Calcimimetic and calcilytic therapies for inherited disorders of the calcium-sensing receptor signalling pathway. Br. J. Pharmacol. 175, 4083–4094 (2018).
pubmed: 29127708 doi: 10.1111/bph.14086
Nemeth, E. F. & Van Wagenen, B. C. Balandrin MF discovery and development of calcimimetic and calcilytic compounds. Prog. Med. Chem. 57, 1–86 (2018).
pubmed: 29680147 doi: 10.1016/bs.pmch.2017.12.001
Conigrave, A. D. & Ward, D. T. Calcium-sensing receptor (CaSR): pharmacological properties and signaling pathways. Best. Pract. Res. Clin. Endocrinol. Metab. 27, 315–331 (2013).
pubmed: 23856262 doi: 10.1016/j.beem.2013.05.010
Yarova, P. L. et al. Calcium-sensing receptor antagonists abrogate airway hyperresponsiveness and inflammation in allergic asthma. Sci. Transl. Med. 7, 284ra260 (2015).
doi: 10.1126/scitranslmed.aaa0282
Schepelmann, M. et al. The vascular Ca2+-sensing receptor regulates blood vessel tone and blood pressure. Am. J. Physiol. Cell Physiol. 310, C193–C204 (2016).
pubmed: 26538090 doi: 10.1152/ajpcell.00248.2015
Roesler, A. M. et al. Calcium sensing receptor in developing human airway smooth muscle. J. Cell Physiol. 234, 14187–14197 (2019).
pubmed: 30624783 pmcid: 6478517 doi: 10.1002/jcp.28115
Smith, K. A. et al. Calcium-sensing receptor regulates cytosolic [Ca (2+)] and plays a major role in the development of pulmonary hypertension. Front. Physiol. 7, 517 (2016).
pubmed: 27867361 pmcid: 5095111 doi: 10.3389/fphys.2016.00517
Kifor, O. et al. Regulation of MAP kinase by calcium-sensing receptor in bovine parathyroid and CaR-transfected HEK293 cells. Am. J. Physiol. Ren. Physiol. 280, F291–F302 (2001).
doi: 10.1152/ajprenal.2001.280.2.F291
Brennan, S. C. et al. The extracellular calcium-sensing receptor regulates human fetal lung development via CFTR. Sci. Rep. 6, 21975 (2016).
pubmed: 26911344 pmcid: 4766410 doi: 10.1038/srep21975
Hartman, W. R. et al. Oxygen dose responsiveness of human fetal airway smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 303, L711–L719 (2012).
pubmed: 22923637 pmcid: 3469631 doi: 10.1152/ajplung.00037.2012
Reyburn, B. et al. The effect of continuous positive airway pressure in a mouse model of hyperoxic neonatal lung injury. Neonatology 109, 6–13 (2016).
pubmed: 26394387 doi: 10.1159/000438818
Vogel, E. R. et al. Perinatal oxygen in the developing lung. Can. J. Physiol. Pharmacol. 93, 119–127 (2015).
pubmed: 25594569 doi: 10.1139/cjpp-2014-0387
Jesudason, E. C. Airway smooth muscle: an architect of the lung? Thorax 64, 541–545 (2009).
pubmed: 19478122 doi: 10.1136/thx.2008.107094
Backstrom, E., Hogmalm, A., Lappalainen, U. & Bry, K. Developmental stage is a major determinant of lung injury in a murine model of bronchopulmonary dysplasia. Pediatr. Res. 69, 312–318 (2011).
pubmed: 21178818 doi: 10.1203/PDR.0b013e31820bcb2a
Fukunaga, T. et al. Prolonged high intermittent positive-pressure ventilation induces airway remodeling and reactivity in young rats. Am. J. Physiol. 275, L567–L573 (1998).
pubmed: 9728052
Liu, M. et al. Stimulation of fetal rat lung cell proliferation in vitro by mechanical stretch. Am. J. Physiol. 263, L376–L383 (1992).
pubmed: 1415562
Zhang, S., Garbutt, V. & McBride, J. T. Strain-induced growth of the immature lung. J. Appl Physiol. 81, 1471–1476 (1996).
pubmed: 8904555 doi: 10.1152/jappl.1996.81.4.1471
Freeman, M. R. et al. Brain-derived neurotrophic factor and airway fibrosis in asthma. Am. J. Physiol. Lung Cell Mol. Physiol. 313, L360–L370 (2017).
pubmed: 28522569 pmcid: 5582935 doi: 10.1152/ajplung.00580.2016
Corrigan, C. J. Calcilytics: a non-steroidal replacement for inhaled steroid and SABA/LABA therapy of human asthma? Expert Rev. Respir. Med. 14, 807–816 (2020).
pubmed: 32306788 doi: 10.1080/17476348.2020.1756779
Tschumperlin, D. J., Ligresti, G., Hilscher, M. B. & Shah, V. H. Mechanosensing and fibrosis. J. Clin. Invest. 128, 74–84 (2018).
pubmed: 29293092 pmcid: 5749510 doi: 10.1172/JCI93561
Tschumperlin, D. J. Mechanotransduction. Compr. Physiol. 1, 1057–1073 (2011).
pubmed: 23737212 doi: 10.1002/cphy.c100016
Liu, F. et al. Mechanosignaling through YAP and TAZ drives fibroblast activation and fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 308, L344–L357 (2015).
pubmed: 25502501 doi: 10.1152/ajplung.00300.2014
Kumawat, K. & Gosens, R. WNT-5A: signaling and functions in health and disease. Cell Mol. Life Sci. 73, 567–587 (2016).
pubmed: 26514730 doi: 10.1007/s00018-015-2076-y

Auteurs

Catherine A Mayer (CA)

Department of Pediatrics, Division of Neonatology, Rainbow Babies & Children's Hospital, Case Western Reserve University, Cleveland, OH, USA.

Benjamin Roos (B)

Department of Anesthesiology and Perioperative Medicine, Mayo Clinic, Rochester, MN, USA.
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.

Jacob Teske (J)

Department of Anesthesiology and Perioperative Medicine, Mayo Clinic, Rochester, MN, USA.
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.

Natalya Wells (N)

Department of Anesthesiology and Perioperative Medicine, Mayo Clinic, Rochester, MN, USA.
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.

Richard J Martin (RJ)

Department of Pediatrics, Division of Neonatology, Rainbow Babies & Children's Hospital, Case Western Reserve University, Cleveland, OH, USA.

Wenhan Chang (W)

Department of Medicine, University of California San Francisco, San Francisco, CA, USA.

Christina M Pabelick (CM)

Department of Anesthesiology and Perioperative Medicine, Mayo Clinic, Rochester, MN, USA.
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.

Y S Prakash (YS)

Department of Anesthesiology and Perioperative Medicine, Mayo Clinic, Rochester, MN, USA. Prakash.ys@mayo.edu.
Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA. Prakash.ys@mayo.edu.

Peter M MacFarlane (PM)

Department of Pediatrics, Division of Neonatology, Rainbow Babies & Children's Hospital, Case Western Reserve University, Cleveland, OH, USA. pmm71@case.edu.

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